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Oxygen Uptake Kinetics

David C. Poole, Andrew M. Jones

10.1002/cphy.c100072

Source: Volume 2, Issue 2, April 2012

Published online: April 2012

Full Article on Wiley Online Library



Abstract

Muscular exercise requires transitions to and from metabolic rates often exceeding an order of magnitude above resting and places prodigious demands on the oxidative machinery and O2‐transport pathway. The science of kinetics seeks to characterize the dynamic profiles of the respiratory, cardiovascular, and muscular systems and their integration to resolve the essential control mechanisms of muscle energetics and oxidative function: a goal not feasible using the steady‐state response. Essential features of the O2 uptake ( o2) kinetics response are highly conserved across the animal kingdom. For a given metabolic demand, fast o2 kinetics mandates a smaller O2 deficit, less substrate‐level phosphorylation and high exercise tolerance. By the same token, slow o2 kinetics incurs a high O2 deficit, presents a greater challenge to homeostasis and presages poor exercise tolerance. Compelling evidence supports that, in healthy individuals walking, running, or cycling upright, o2 kinetics control resides within the exercising muscle(s) and is therefore not dependent upon, or limited by, upstream O2‐transport systems. However, disease, aging, and other imposed constraints may redistribute o2 kinetics control more proximally within the O2‐transport system. Greater understanding of o2 kinetics control and, in particular, its relation to the plasticity of the O2‐transport/utilization system is considered important for improving the human condition, not just in athletic populations, but crucially for patients suffering from pathologically slowed o2 kinetics as well as the burgeoning elderly population. © 2012 American Physiological Society. Compr Physiol 2:933‐996, 2012.

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Figure 1. Figure 1.

Profiles of children's (6‐10 year olds) o2 during free ranging spontaneous activity. These have been ranked as low, moderate, and heavy activity for (A) (female), (B) (female), and (C) (male), children respectively. Horizontal line denotes the gas exchange threshold, GET.

Redrawn, with permission, from Bailey et al. (22).
Figure 2. Figure 2.

With respect to the speed of o2 kinetics there are O2‐delivery‐dependent and ‐independent regions. Note that when O2 delivery falls below the “tipping point” o2 kinetics becomes progressively slowed as evidenced by increasing τ (see inset for graphical portrayal of altered τ). In young healthy individuals conventional locomotory activities such as walking, running, and cycling lie to the right of the tipping point. Many diseases such as chronic heart failure, emphysema [chronic obstructive pulmonary disease (COPD)] and type II diabetes (see Section Disease States) as well as healthy aging (see Section Maturation and Aging) move the individual leftward into the O2‐delivery‐dependent region.
Figure 3. Figure 3.

The pathway for O2 from lung to skeletal muscle mitochondria. For healthy humans performing large muscle mass exercise (e.g., cycling and running) o2 kinetics at exercise onset are controlled by the capacity for mitochondrial O2 utilization (right‐most arrow) rather than upstream perfusive or diffusive flux limitations (larger arrows, left and middle) as is the case for o2max [see Section Site(s) of Limitation of o2 Kinetics: Oxygen Delivery Versus Cellular Respiration for more details).
Figure 4. Figure 4.

Two of the foremost pioneers in the field of exercise metabolic control and o2 kinetics. Left panel: Nobel laureate Archibald Vivian Hill in 1927. Right panel: Brian J. Whipp in 2002.
Figure 5. Figure 5.

o2 response following the onset of moderate (<gas exchange threshold, GET), heavy (>GET<critical power, CP), severe (>CP leading to o2max), and extreme (>severe such that fatigue ensues before o2max is achieved) exercise. Note that for moderate exercise a steady state is achieved rapidly; for heavy exercise the steady state is delayed; for severe exercise no steady state is evident but o2 projects to o2max which is achieved before fatigue ensues (arrows). Both heavy and severe exercise may evince a slow component (i.e., o2sc see Section Slow Component of o2 Kinetics: Mechanistic Bases). For extreme exercise, fatigue ensues prior to reaching o2max.

Adapted, with permission, from Wilkerson et al. (788).
Figure 6. Figure 6.

Top: breath‐by‐breath alveolar o2 response following the onset of moderate intensity cycle ergometer exercise. Phases I (cardiodynamic), II (primary), and III (steady‐state) are designated and fit by an appropriate exponential model (see text). Bottom: schematic demonstrating fundamental properties of the single component exponential response. Note that the imposition of a time delay feature (omitted here for clarity) is required to improve the model fit and account for Phase I (see Eq. 5). The rate of o2 increase is quantified by the time constant (τ) of the exponential (∼40 s for this example) where BL signifies baseline o2 and Δ the increase or amplitude of o2 above baseline (right vertical arrows, ∼2 liters·min−1 for this example). For each multiple of τ o2 increases by 63% of the difference between that value at the previous τ and the required steady state. Thus, after 2τ (∼80 s) o2 has risen to 86%Δ [1.0−0.63 = 0.37; (0.37 × 0.63) + 0.63 = 0.86], 3τ's (∼120 s) = 95%Δ, 4τ's (∼160 s) = 98%Δ. τp designates the time constant of the primary component response. Also shown is the metabolic error signal [difference between o2(t) and Δ that drives the increase of o2] which decreases with each increment of τ. The O2 deficit is the area from exercise onset (time = 0) bounded by the actual o2 profile and the asymptotic o2 projected backward to time 0.
Figure 7. Figure 7.

Left panel: schematic representation of the o2 response to constant‐work‐rate exercise in the moderate, heavy, and severe domains. Note presence of o2 slow component (hatched area) for heavy and severe exercise. Arrow denotes exercise curtailed by fatigue. Right panel: schematic representation of the blood [lactate] response to constant‐work‐rate exercise in the moderate, heavy, and severe domains. Arrow denotes exercise curtailed by fatigue. Note correspondence between [lactate] and o2 responses within domains.
Figure 8. Figure 8.

Left panel: schematic of ventilatory (E) response following the onset of moderate intensity exercise. Phases I, II and III are demarcated. Center panels: breath‐by‐breath responses of E, CO2 output (CO2), O2 uptake (o2), and heart rate (HR) to a single bout of 100‐W (moderate) exercise from rest. The group mean time constants of the responses were 29 (o2), 51 (CO2), and 54 s (E). Note the almost instantaneous Phase I increases in E and pulmonary gas exchange as well as very rapid HR kinetics following exercise onset. See text for more details. Vertical line indicates onset of exercise. Adapted, with permission, from Whipp et al. (769). Right panel: schematic overlaying time courses of E, CO2, and o2. E tracks CO2 which is far slower than o2 due to higher solubility and tissue storage of of CO2. One consequence of this behavior is a transient decrease of end‐tidal Po2 and a mild arterial hypoxemia. See text for more details.
Figure 9. Figure 9.

Relative increase in femoral artery blood flow (solid line) compared with alveolar o2 (dotted line) across the transient from unloaded to heavy intensity knee extension exercise. Note far faster blood flow (mean response time, MRT, 46 s) than o2 (MRT, 69 s) response. Redrawn from Koga et al. (432), with permission.
Figure 10. Figure 10.

Vasodilator dynamics of isolated arterioles from the soleus and red gastrocnemius muscles of young rats to intraluminal flow (∼13 nl/s) and acetylcholine (Ach, 1 × 10−6 M). Exposure to each condition was initiated at time 0. Adapted, with permission, from the data of Behnke and Delp (66).
Figure 11. Figure 11.

Pulmonary (alveolar) and leg muscle o2 response to moderate intensity cycling for one subject. Note that, in the original investigation four of six subjects demonstrated a brief period following the onset of work where leg “muscle” o2 did not increase. See Grassi (273 and 285) for all individual and mean responses. Arrow (and open diamonds) denotes time taken to reach 50% of final response. Inset: the consequence of blood flow increasing faster than o2 is a transient reduction in fractional O2 extraction. Redrawn, with permission, from Grassi et al. (285).
Figure 12. Figure 12.

Relative increase in time‐aligned alveolar (solid line) and leg muscle (dashed line) o2 across the transient from unloaded to heavy‐intensity knee‐extension exercise. Note strong similarity in time courses. Redrawn, with permission, from Koga et al. (432).
Figure 13. Figure 13.

Pulmonary o2 (solid circles) and intramuscular [PCr] (expressed as a relative change from baseline of 100% and “flipped” to facilitate more direct comparison with the o2 responses; hollow circles) kinetic responses during and following moderate‐ and heavy‐intensity square‐wave exercise transitions. The on‐responses are phase‐aligned (dashed vertical lines) to account for the muscle‐to‐lung transit time. All responses are fit with a monoexponential curve (dashed curves) with the exception of the o2 slow component behavior evident only for the high intensity on transition (i.e., lower left). Note exceptionally close correspondence between o2 and [PCr] responses in all instances. Redrawn, with permission, from Rossiter et al. (645).
Figure 14. Figure 14.

Mean data for increase in rat spinotrapezius red blood cell (RBC) flux (upper) and microvascular Po2 (middle) are conflated to estimate o2 (lower) in response to 1 Hz contractions. Model fits are shown. Both RBC flux and o2 (but not Pmvo2) were fit by a single exponential with no delay. TD, time delay. τ, time constant. Redrawn, with permission, from Behnke et al. (64).
Figure 15. Figure 15.

o2 (jagged curve) time delay and monoexponential fit (smooth curve) as determined in a single isolated myocyte from Xenopus laevis lumbrical muscle in response to 3 min of isometric tetanic contractions (1 Hz). Kinetics analysis evidenced no time delay prior to the increase of o2 and far more rapid muscle than pulmonary o2 kinetics in amphibians. Figure redrawn, with permission, from Kindig and colleagues (423).
Figure 16. Figure 16.

Microvascular O2 partial pressure (Pmvo2) responses for soleus (slow twitch) and the mixed and white gastrocnemii (both fast twitch) during high‐intensity electrical stimulation at 1 Hz beginning at time = 0 s. Thin line is actual data, thick line denotes model fit. Note the “undershoot” in both of the fast‐twitch muscle responses and also the much lower contracting Pmvo2. Redrawn, with permission, from McDonough et al. (512).
Figure 17. Figure 17.

Relative increases in quadriceps muscle deoxygenation [deoxy(Hb+Mb)] (solid lines) for ten sites (measured by near infrared spectroscopy) and pulmonary o2 (dashed line, note comparatively slower response) during heavy exercise. Values are normalized to end‐exercise increase over baseline. Subjects shown had the least (top) and most (bottom) intersite heterogeneity of group. Thick line denotes response at the single site most often studied. Adapted, with permission, from Koga et al. (431). See text for details.
Figure 18. Figure 18.

Pulmonary o2 responses to an initial (solid circles) and subsequent (i.e., primed, hollow circles) heavy exercise bouts separated by 12 min. Data are averaged and superimposed. Redrawn, with permission, from data of Burnley et al. (106). Note increased amplitude of o2 primary component and reduced o2 slow component.
Figure 19. Figure 19.

Left: o2—work‐rate relation for incremental exercise (25 Watts min−1 to fatigue, solid symbols and line) and o2 achieved during constant‐work‐rate exercise (hollow symbols) for a representative healthy subject. The leftmost hollow symbol denotes o2 at 24 min of heavy exercise (at critical power, CP); all others are at fatigue in the severe domain (>CP) where o2 achieves its maximum value. Right: schematic demonstrating the magnitude of the o2 slow component as calculated from the vertical displacement of constant‐work‐rate o2's (hollow symbols) from their respective iso‐work‐rate counterparts measured during incremental exercise (solid symbols) in left panel. Note that, for this subject, the o2 slow component peaks ∼1.5 liter O2 min−1. Constructed, with permission, from the data of Poole et al. (610).
Figure 20. Figure 20.

o2 slow component increases O2 cost of constant‐work‐rate exercise and reduces efficiency of work for all supra‐gas exchange threshold (GET) work rates. Redrawn, with permission, from the data of Henson et al. (330).
Figure 21. Figure 21.

Relative contribution of the o2 slow component to end‐exercise o2 during 6 min of heavy‐intensity cycle exercise plotted as a function of vastus lateralis % type I muscle fibers. Data extracted, with permission, from Barstow et al. (39), Pringle et al. (616), and Carter et al. (124).
Figure 22. Figure 22.

Thigh o2 response to knee‐extension exercise under control (solid symbols) and with preferential CUR of type I fibers (cisatracurium, hollow symbols). Values are means (SE omitted for clarity, n = 8). Redrawn, with permission, from Krustrup et al. (456). *CUR P < 0.05 versus control.
Figure 23. Figure 23.

Current array of putative mediators of o2 slow component which has been severely truncated since 1980. See text for further details.
Figure 24. Figure 24.

Pulmonary o2 response to arm cranking versus leg cycle ergometer exercise scaled to end exercise o2. Redrawn, with permission, from Koppo et al. (441).
Figure 25. Figure 25.

o2 kinetics across species portrayed as the time taken to reach 63% of the final o2 (i.e., τ here is synonymous with mean response time, MRT) and the mass‐specific o2max. Note that, in most species, distinction between Phase I and the primary component was not possible. Inset features the mammalian species separately. Redrawn, with permission, from Poole et al. (602).
Figure 26. Figure 26.

Comparison of o2 response among the Thoroughbred horse, untrained human, and toad following a stepwise increase in metabolic demand.
Figure 27. Figure 27.

o2 kinetics following onset of heavy‐intensity cycle exercise in subjects with a high proportion of type I (solid circles) and type II (hollow circles) in their quadriceps muscles.

Reproduced, with permission, from Barstow et al. (39).
Figure 28. Figure 28.

Schematic illustration of o2 kinetics (expressed as o2 per Watt, i.e., gain, G) following onset of heavy‐intensity exercise at pedal rates of 35, 75, and 115 rpm. Note the progressive fall in primary component gain (Gp) and increased o2 slow component with faster speeds expected to recruit more type II fibers (compare with Fig. 27). Moderate exercise at 75 rpm is shown for comparison.

Reproduced, with permission, from Pringle et al. (617).
Figure 29. Figure 29.

Conceptual model exploring recruitment of muscle fiber populations with varying metabolic characteristics on the o2 response to heavy (>gas exchange threshold, GET, but <critical power, CP, top) and severe (i.e., > CP, bottom) exercise. Solid lines denote responses of muscle fibers having relatively fast kinetics and high “efficiency” (low gain, G), and dashed lines those fibers with comparatively slow kinetics and high G. These two disparate fiber populations are notionally equivalent to type I and type II fibers, respectively. The overall o2 response is given by the bolded solid line. Note the slow component that eventually stabilizes for heavy exercise (top) but not for severe exercise where o2 projects toward o2max (bottom). Hypothetically, these disparate behaviors might be explained by severe exercise mandating a progressive recruitment of additional higher‐order fibers (which is not seen for heavy exercise): Though, as discussed in the text, this is not a requirement. Redrawn, with permission, from Wilkerson and Jones (787).
Figure 30. Figure 30.

Group mean o2 cost (expressed as ml O2 min −1W−1) for moderate‐ (left panel) and heavy/severe‐ (right panel) intensity exercise in children and adults. Note that for moderate‐intensity exercise and in the first several minutes of heavy/severe‐intensity exercise the O2 cost or gain (G) is far greater in children. Also, for heavy/severe exercise there is a pronounced o2 slow component in adults that appears largely absent in the children who exhibit a far greater primary component G. Adapted from Armon et al. (7), with permission.
Figure 31. Figure 31.

Effects of maturation and aging on primary component o2 kinetics (τp) in healthy males and females. Solid symbols, black regression curve with 95% confidence interval (dashed lines) denote mean data from references 76, 145, 233, 542, 674, and 769 for untrained subjects. Open circles and blue dashed regression curve are adapted, with permission, from Berger et al. (80) for endurance‐trained track athletes. Notice that, unlike for o2max (14, 513), the age‐related decline in o2 kinetics (i.e., slower τp) appears to be almost completely curtailed by endurance training, at least in some individuals. Open triangles are from a rare longtudinal study where six males and one female were tested 9 years apart (76). For these individuals, despite the absence of overt disease, τp slows at a rate (i.e., 1.8 s/year) that was several‐fold greater than that calculated from the other investigations.
Figure 32. Figure 32.

Marked slowing of o2 kinetics in chronic obstructive pulmonary disease (COPD) following the onset of moderate intensity cycle exercise compared with age‐matched control subjects. Drawn, with permission, from data of Nery et al. (542).
Figure 33. Figure 33.

Left panel: mean o2 response following the onset of unloaded (0 Watt) cycling in patients with cyanotic congenital heart disease compared with age‐matched healthy control subjects. Shaded area denotes Phase I. Right panel: magnitude of the Phase I o2 (cardiodynamic component) in ml O2. Redrawn, with permission, from Sietsema et al. (689).
Figure 34. Figure 34.

Red blood cell (RBC) flux following the onset of 1 Hz contractions of the rat spinotrapezius muscle in control and chronic heart failure (CHF) animals. Data taken from Kindig et al. (428) and Richardson et al. (629), with permission.
Figure 35. Figure 35.

Time constants (τp) of pulmonary o2 kinetics in mitochondrial myopathy and McArdle's disease patients are negatively related (r = 0.81, P<0.05) to the near infrared spectroscopy‐derived muscle deoxygenation index (Δ[deoxy(Hb + Mb]peak]) (estimate of muscle fractional O2 extraction) during cycle ergometry. Healthy control subject data also shown for comparison. Reconstructed, with permission, from the data of Grassi et al. (286).
Figure 36. Figure 36.

o2 kinetics following the onset of moderate‐intensity cycle exercise (230 Watts) in a Belgian junior cycle champion. The time constant (τp) of the primary component response is a remarkable 9 s, close to that found in Paula Radcliffe, the World record holder in the women's marathon as well as in Thoroughbred horses.
Figure 37. Figure 37.

The training‐induced speeding of o2 kinetics evidenced from the time‐to‐90% of steady‐state response [top panel, redrawn, with permission, from Hickson et al. (339)] results from a speeding of the primary o2 response time constant [τpo2, see lower left panel redrawn, with permission, from data of Phillips et al. (576)] and, a reduction in the size of the o2 slow component [i.e., above the gas exchange threshold, GET, right panel redrawn, with permission, from Womack et al. (795)].


Figure 1.

Profiles of children's (6‐10 year olds) o2 during free ranging spontaneous activity. These have been ranked as low, moderate, and heavy activity for (A) (female), (B) (female), and (C) (male), children respectively. Horizontal line denotes the gas exchange threshold, GET.

Redrawn, with permission, from Bailey et al. (22).


Figure 2.

With respect to the speed of o2 kinetics there are O2‐delivery‐dependent and ‐independent regions. Note that when O2 delivery falls below the “tipping point” o2 kinetics becomes progressively slowed as evidenced by increasing τ (see inset for graphical portrayal of altered τ). In young healthy individuals conventional locomotory activities such as walking, running, and cycling lie to the right of the tipping point. Many diseases such as chronic heart failure, emphysema [chronic obstructive pulmonary disease (COPD)] and type II diabetes (see Section Disease States) as well as healthy aging (see Section Maturation and Aging) move the individual leftward into the O2‐delivery‐dependent region.



Figure 3.

The pathway for O2 from lung to skeletal muscle mitochondria. For healthy humans performing large muscle mass exercise (e.g., cycling and running) o2 kinetics at exercise onset are controlled by the capacity for mitochondrial O2 utilization (right‐most arrow) rather than upstream perfusive or diffusive flux limitations (larger arrows, left and middle) as is the case for o2max [see Section Site(s) of Limitation of o2 Kinetics: Oxygen Delivery Versus Cellular Respiration for more details).



Figure 4.

Two of the foremost pioneers in the field of exercise metabolic control and o2 kinetics. Left panel: Nobel laureate Archibald Vivian Hill in 1927. Right panel: Brian J. Whipp in 2002.



Figure 5.

o2 response following the onset of moderate (<gas exchange threshold, GET), heavy (>GET<critical power, CP), severe (>CP leading to o2max), and extreme (>severe such that fatigue ensues before o2max is achieved) exercise. Note that for moderate exercise a steady state is achieved rapidly; for heavy exercise the steady state is delayed; for severe exercise no steady state is evident but o2 projects to o2max which is achieved before fatigue ensues (arrows). Both heavy and severe exercise may evince a slow component (i.e., o2sc see Section Slow Component of o2 Kinetics: Mechanistic Bases). For extreme exercise, fatigue ensues prior to reaching o2max.

Adapted, with permission, from Wilkerson et al. (788).


Figure 6.

Top: breath‐by‐breath alveolar o2 response following the onset of moderate intensity cycle ergometer exercise. Phases I (cardiodynamic), II (primary), and III (steady‐state) are designated and fit by an appropriate exponential model (see text). Bottom: schematic demonstrating fundamental properties of the single component exponential response. Note that the imposition of a time delay feature (omitted here for clarity) is required to improve the model fit and account for Phase I (see Eq. 5). The rate of o2 increase is quantified by the time constant (τ) of the exponential (∼40 s for this example) where BL signifies baseline o2 and Δ the increase or amplitude of o2 above baseline (right vertical arrows, ∼2 liters·min−1 for this example). For each multiple of τ o2 increases by 63% of the difference between that value at the previous τ and the required steady state. Thus, after 2τ (∼80 s) o2 has risen to 86%Δ [1.0−0.63 = 0.37; (0.37 × 0.63) + 0.63 = 0.86], 3τ's (∼120 s) = 95%Δ, 4τ's (∼160 s) = 98%Δ. τp designates the time constant of the primary component response. Also shown is the metabolic error signal [difference between o2(t) and Δ that drives the increase of o2] which decreases with each increment of τ. The O2 deficit is the area from exercise onset (time = 0) bounded by the actual o2 profile and the asymptotic o2 projected backward to time 0.



Figure 7.

Left panel: schematic representation of the o2 response to constant‐work‐rate exercise in the moderate, heavy, and severe domains. Note presence of o2 slow component (hatched area) for heavy and severe exercise. Arrow denotes exercise curtailed by fatigue. Right panel: schematic representation of the blood [lactate] response to constant‐work‐rate exercise in the moderate, heavy, and severe domains. Arrow denotes exercise curtailed by fatigue. Note correspondence between [lactate] and o2 responses within domains.



Figure 8.

Left panel: schematic of ventilatory (E) response following the onset of moderate intensity exercise. Phases I, II and III are demarcated. Center panels: breath‐by‐breath responses of E, CO2 output (CO2), O2 uptake (o2), and heart rate (HR) to a single bout of 100‐W (moderate) exercise from rest. The group mean time constants of the responses were 29 (o2), 51 (CO2), and 54 s (E). Note the almost instantaneous Phase I increases in E and pulmonary gas exchange as well as very rapid HR kinetics following exercise onset. See text for more details. Vertical line indicates onset of exercise. Adapted, with permission, from Whipp et al. (769). Right panel: schematic overlaying time courses of E, CO2, and o2. E tracks CO2 which is far slower than o2 due to higher solubility and tissue storage of of CO2. One consequence of this behavior is a transient decrease of end‐tidal Po2 and a mild arterial hypoxemia. See text for more details.



Figure 9.

Relative increase in femoral artery blood flow (solid line) compared with alveolar o2 (dotted line) across the transient from unloaded to heavy intensity knee extension exercise. Note far faster blood flow (mean response time, MRT, 46 s) than o2 (MRT, 69 s) response. Redrawn from Koga et al. (432), with permission.



Figure 10.

Vasodilator dynamics of isolated arterioles from the soleus and red gastrocnemius muscles of young rats to intraluminal flow (∼13 nl/s) and acetylcholine (Ach, 1 × 10−6 M). Exposure to each condition was initiated at time 0. Adapted, with permission, from the data of Behnke and Delp (66).



Figure 11.

Pulmonary (alveolar) and leg muscle o2 response to moderate intensity cycling for one subject. Note that, in the original investigation four of six subjects demonstrated a brief period following the onset of work where leg “muscle” o2 did not increase. See Grassi (273 and 285) for all individual and mean responses. Arrow (and open diamonds) denotes time taken to reach 50% of final response. Inset: the consequence of blood flow increasing faster than o2 is a transient reduction in fractional O2 extraction. Redrawn, with permission, from Grassi et al. (285).



Figure 12.

Relative increase in time‐aligned alveolar (solid line) and leg muscle (dashed line) o2 across the transient from unloaded to heavy‐intensity knee‐extension exercise. Note strong similarity in time courses. Redrawn, with permission, from Koga et al. (432).



Figure 13.

Pulmonary o2 (solid circles) and intramuscular [PCr] (expressed as a relative change from baseline of 100% and “flipped” to facilitate more direct comparison with the o2 responses; hollow circles) kinetic responses during and following moderate‐ and heavy‐intensity square‐wave exercise transitions. The on‐responses are phase‐aligned (dashed vertical lines) to account for the muscle‐to‐lung transit time. All responses are fit with a monoexponential curve (dashed curves) with the exception of the o2 slow component behavior evident only for the high intensity on transition (i.e., lower left). Note exceptionally close correspondence between o2 and [PCr] responses in all instances. Redrawn, with permission, from Rossiter et al. (645).



Figure 14.

Mean data for increase in rat spinotrapezius red blood cell (RBC) flux (upper) and microvascular Po2 (middle) are conflated to estimate o2 (lower) in response to 1 Hz contractions. Model fits are shown. Both RBC flux and o2 (but not Pmvo2) were fit by a single exponential with no delay. TD, time delay. τ, time constant. Redrawn, with permission, from Behnke et al. (64).



Figure 15.

o2 (jagged curve) time delay and monoexponential fit (smooth curve) as determined in a single isolated myocyte from Xenopus laevis lumbrical muscle in response to 3 min of isometric tetanic contractions (1 Hz). Kinetics analysis evidenced no time delay prior to the increase of o2 and far more rapid muscle than pulmonary o2 kinetics in amphibians. Figure redrawn, with permission, from Kindig and colleagues (423).



Figure 16.

Microvascular O2 partial pressure (Pmvo2) responses for soleus (slow twitch) and the mixed and white gastrocnemii (both fast twitch) during high‐intensity electrical stimulation at 1 Hz beginning at time = 0 s. Thin line is actual data, thick line denotes model fit. Note the “undershoot” in both of the fast‐twitch muscle responses and also the much lower contracting Pmvo2. Redrawn, with permission, from McDonough et al. (512).



Figure 17.

Relative increases in quadriceps muscle deoxygenation [deoxy(Hb+Mb)] (solid lines) for ten sites (measured by near infrared spectroscopy) and pulmonary o2 (dashed line, note comparatively slower response) during heavy exercise. Values are normalized to end‐exercise increase over baseline. Subjects shown had the least (top) and most (bottom) intersite heterogeneity of group. Thick line denotes response at the single site most often studied. Adapted, with permission, from Koga et al. (431). See text for details.



Figure 18.

Pulmonary o2 responses to an initial (solid circles) and subsequent (i.e., primed, hollow circles) heavy exercise bouts separated by 12 min. Data are averaged and superimposed. Redrawn, with permission, from data of Burnley et al. (106). Note increased amplitude of o2 primary component and reduced o2 slow component.



Figure 19.

Left: o2—work‐rate relation for incremental exercise (25 Watts min−1 to fatigue, solid symbols and line) and o2 achieved during constant‐work‐rate exercise (hollow symbols) for a representative healthy subject. The leftmost hollow symbol denotes o2 at 24 min of heavy exercise (at critical power, CP); all others are at fatigue in the severe domain (>CP) where o2 achieves its maximum value. Right: schematic demonstrating the magnitude of the o2 slow component as calculated from the vertical displacement of constant‐work‐rate o2's (hollow symbols) from their respective iso‐work‐rate counterparts measured during incremental exercise (solid symbols) in left panel. Note that, for this subject, the o2 slow component peaks ∼1.5 liter O2 min−1. Constructed, with permission, from the data of Poole et al. (610).



Figure 20.

o2 slow component increases O2 cost of constant‐work‐rate exercise and reduces efficiency of work for all supra‐gas exchange threshold (GET) work rates. Redrawn, with permission, from the data of Henson et al. (330).



Figure 21.

Relative contribution of the o2 slow component to end‐exercise o2 during 6 min of heavy‐intensity cycle exercise plotted as a function of vastus lateralis % type I muscle fibers. Data extracted, with permission, from Barstow et al. (39), Pringle et al. (616), and Carter et al. (124).



Figure 22.

Thigh o2 response to knee‐extension exercise under control (solid symbols) and with preferential CUR of type I fibers (cisatracurium, hollow symbols). Values are means (SE omitted for clarity, n = 8). Redrawn, with permission, from Krustrup et al. (456). *CUR P < 0.05 versus control.



Figure 23.

Current array of putative mediators of o2 slow component which has been severely truncated since 1980. See text for further details.



Figure 24.

Pulmonary o2 response to arm cranking versus leg cycle ergometer exercise scaled to end exercise o2. Redrawn, with permission, from Koppo et al. (441).



Figure 25.

o2 kinetics across species portrayed as the time taken to reach 63% of the final o2 (i.e., τ here is synonymous with mean response time, MRT) and the mass‐specific o2max. Note that, in most species, distinction between Phase I and the primary component was not possible. Inset features the mammalian species separately. Redrawn, with permission, from Poole et al. (602).



Figure 26.

Comparison of o2 response among the Thoroughbred horse, untrained human, and toad following a stepwise increase in metabolic demand.



Figure 27.

o2 kinetics following onset of heavy‐intensity cycle exercise in subjects with a high proportion of type I (solid circles) and type II (hollow circles) in their quadriceps muscles.

Reproduced, with permission, from Barstow et al. (39).


Figure 28.

Schematic illustration of o2 kinetics (expressed as o2 per Watt, i.e., gain, G) following onset of heavy‐intensity exercise at pedal rates of 35, 75, and 115 rpm. Note the progressive fall in primary component gain (Gp) and increased o2 slow component with faster speeds expected to recruit more type II fibers (compare with Fig. 27). Moderate exercise at 75 rpm is shown for comparison.

Reproduced, with permission, from Pringle et al. (617).


Figure 29.

Conceptual model exploring recruitment of muscle fiber populations with varying metabolic characteristics on the o2 response to heavy (>gas exchange threshold, GET, but <critical power, CP, top) and severe (i.e., > CP, bottom) exercise. Solid lines denote responses of muscle fibers having relatively fast kinetics and high “efficiency” (low gain, G), and dashed lines those fibers with comparatively slow kinetics and high G. These two disparate fiber populations are notionally equivalent to type I and type II fibers, respectively. The overall o2 response is given by the bolded solid line. Note the slow component that eventually stabilizes for heavy exercise (top) but not for severe exercise where o2 projects toward o2max (bottom). Hypothetically, these disparate behaviors might be explained by severe exercise mandating a progressive recruitment of additional higher‐order fibers (which is not seen for heavy exercise): Though, as discussed in the text, this is not a requirement. Redrawn, with permission, from Wilkerson and Jones (787).



Figure 30.

Group mean o2 cost (expressed as ml O2 min −1W−1) for moderate‐ (left panel) and heavy/severe‐ (right panel) intensity exercise in children and adults. Note that for moderate‐intensity exercise and in the first several minutes of heavy/severe‐intensity exercise the O2 cost or gain (G) is far greater in children. Also, for heavy/severe exercise there is a pronounced o2 slow component in adults that appears largely absent in the children who exhibit a far greater primary component G. Adapted from Armon et al. (7), with permission.



Figure 31.

Effects of maturation and aging on primary component o2 kinetics (τp) in healthy males and females. Solid symbols, black regression curve with 95% confidence interval (dashed lines) denote mean data from references 76, 145, 233, 542, 674, and 769 for untrained subjects. Open circles and blue dashed regression curve are adapted, with permission, from Berger et al. (80) for endurance‐trained track athletes. Notice that, unlike for o2max (14, 513), the age‐related decline in o2 kinetics (i.e., slower τp) appears to be almost completely curtailed by endurance training, at least in some individuals. Open triangles are from a rare longtudinal study where six males and one female were tested 9 years apart (76). For these individuals, despite the absence of overt disease, τp slows at a rate (i.e., 1.8 s/year) that was several‐fold greater than that calculated from the other investigations.



Figure 32.

Marked slowing of o2 kinetics in chronic obstructive pulmonary disease (COPD) following the onset of moderate intensity cycle exercise compared with age‐matched control subjects. Drawn, with permission, from data of Nery et al. (542).



Figure 33.

Left panel: mean o2 response following the onset of unloaded (0 Watt) cycling in patients with cyanotic congenital heart disease compared with age‐matched healthy control subjects. Shaded area denotes Phase I. Right panel: magnitude of the Phase I o2 (cardiodynamic component) in ml O2. Redrawn, with permission, from Sietsema et al. (689).



Figure 34.

Red blood cell (RBC) flux following the onset of 1 Hz contractions of the rat spinotrapezius muscle in control and chronic heart failure (CHF) animals. Data taken from Kindig et al. (428) and Richardson et al. (629), with permission.



Figure 35.

Time constants (τp) of pulmonary o2 kinetics in mitochondrial myopathy and McArdle's disease patients are negatively related (r = 0.81, P<0.05) to the near infrared spectroscopy‐derived muscle deoxygenation index (Δ[deoxy(Hb + Mb]peak]) (estimate of muscle fractional O2 extraction) during cycle ergometry. Healthy control subject data also shown for comparison. Reconstructed, with permission, from the data of Grassi et al. (286).



Figure 36.

o2 kinetics following the onset of moderate‐intensity cycle exercise (230 Watts) in a Belgian junior cycle champion. The time constant (τp) of the primary component response is a remarkable 9 s, close to that found in Paula Radcliffe, the World record holder in the women's marathon as well as in Thoroughbred horses.



Figure 37.

The training‐induced speeding of o2 kinetics evidenced from the time‐to‐90% of steady‐state response [top panel, redrawn, with permission, from Hickson et al. (339)] results from a speeding of the primary o2 response time constant [τpo2, see lower left panel redrawn, with permission, from data of Phillips et al. (576)] and, a reduction in the size of the o2 slow component [i.e., above the gas exchange threshold, GET, right panel redrawn, with permission, from Womack et al. (795)].

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Article Title: Oxygen Uptake Kinetics
 

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David C. Poole, Andrew M. Jones. Oxygen Uptake Kinetics. Compr Physiol 2012, 2: 933-996. doi: 10.1002/cphy.c100072